Science Tribune - Article - August 1996
Time to drastically change the century-old concept about bacteria
L.G. Mathieu and S. Sonea
Department of Microbiology and Immunology, University of Montreal, P.O. Box 6128, Station "Centre-ville", Montreal, Quebec H3C 3J7, Canada
Key words: bacteria, changed-concept, bacterial global network
Knowledge of bacteria has developed in such a way that the biological community has originally formed and accepted an erroneous image of the bacterial way of life. Past generations of students have toiled with somewhat confusing and at times inexact notions on bacteria (1) (2) with the result that many of them became indifferent to proposals for new concepts and some even refractory to bacteriology itself. The latter has thus become a scientific Cinderella. Only the successive accumulation of scientific proofs from all over the world has recently awakened a small number of biologists to the bacterial world as a major and essential part of our biosphere, able of entirely original formulas which, by the interplay of generalized solidarity, make every bacterium a participant in and a beneficiary of the global, powerful bacterial superorganism.
Disease-causing bacteria were the first to be systematically studied
The erroneous perception of the bacterial world can be explained. The first bacteria which were systematically studied were those responsible for the dreaded infectious diseases, main cause of mortality in the 19th century. The prestige of scientists like Pasteur, Koch and others working so successfully with infectious bacteria was great and their decision to consider different types as separate species was not questioned from about 1870 on. These strains were parasitic of human tissues and could be grown in the laboratory in sterilized, soup-like extracts of common meats. Once isolated, they grew well in pure cultures and could be further studied. Each type of strain isolated from infected humans or domestic animals was considered a species.
The significance of bacteria's entirely original adaptive mechanisms was not perceived easily
It was only later that successive discoveries indicated that the bacterial world is original and more complex than initial observations on parasitic strains had led bacteriologists to believe. Early in this century, the soil microbiologists described a completely different way of bacterial life: soil bacteria associated in teams of many cooperative types of strains. Few of them (probably less than 1%) could be artificially grown and isolated in pure cultures from the companion strains of their natural habitat. These reciprocally supporting strains need each other and behave like the specialized cells of an animal. It was only gradually that soil bacteria, millions of times more numerous than the infectious ones, were accepted as specialized elements of a successful type of a local, complex "organism", the bacterial team. Still later, environmental bacteriologists came to realize that by their collective metabolic activities, individual bacterial teams stabilize their environment, fertilize the soil and, together, sustain the entire biosphere.
A second indication that bacteria possessed very original adaptive mechanisms was the discovery that they could help each other with hereditary information carried by a chemical substance (DNA) in a non-Mendelian way. In 1928, Griffith observed that pneumococci that killed mice experimentally could, even when dead, transfer this capacity to other strains that were previously shown unable to attack mice, and which integrated it in their own heredity (transformation). This extraordinary gene transfer process was subsequently repeated rather easily with many other types of bacteria.
In the 40's and 50's another series of experimental discoveries showed other entirely original processes of gene exchanges between bacterial strains. In these cases, the genes which passed on from one strain to the other were organized in circular, self-replicating DNA molecules, plasmids and prophages. The latter were shown to carry "converting" genes (non essential but potentially useful). In addition, they could transport any other genetic material from their former host bacterium (transduction). Although several Nobel prizes were eventually granted for early work on both types of self-transmissible DNA molecules, these were nonetheless considered for many years as mere curiosities. In 1963 however, well known bacteria causing severe bacterial intestinal infections with a high mortality rate appeared in different countries, each bacterial strain involved having acquired resistance to four or five commonly used antibacterial drugs, particularly antibiotics. Their multiple resistance was due to genes originally carried by soil bacteria and which were transferred from one strain to another and eventually to infectious ones by self-transmissible "resistance" (R) plasmids (3). Soon it became evident that in other types of bacterial infections the prophages had also transferred resistance genes, usually by transduction. The infectious bacteria which still were considered typical species living in genetic isolation suddenly made it evident that they too were benefitting from the common, global reserve of all bacterial genes from which they could "borrow" supplementary information; they were therefore beneficiaries of the entire bacterial world. Numerous other reports of infectious resistance were published. These alarming observations marked the beginning of acceptance that bacteria were not genetically isolated species like the eukaryotes; rather they lived in an open gene market (4). Today, most medical microbiologists agree that effective antibacterial drugs of yesteryears must be used discriminately since infectious bacteria have access to resistance genes from all over. Ecologists discovered that a similar situation could exist in other habitats. Bacteria exposed to natural or industrial toxic substances often become more resistant through the acquisition of genes transferred to them by plasmids or temperate phages.
Bacteria participate in a global communication system
The ability of bacteria to adapt and survive by resorting to the temporary transfers of genes from different bacterial strains should be perceived as a generalized phenomenon. It reflects a way of life based on widespread solidarity, typically bacterial, and unknown in eukaryotes. We compare this generalized and frequent exchange of bacterial genes between strains to a unified global bacterial communication system like a biological Internet (1) (5) (6). Each bacterium behaves as a two way broadcasting element: it displays surface receptors to facilitate the selective binding of visitor genes and it carries, for its own benefit and that of others, at least one self-replicating circular DNA molecule (prophage or plasmid).
This type of genetic solidarity is seconded by the successful and generalized facility of bacteria to associate in teams. Today's highly specialized types of bacterial cells are the result of a long evolution characterized by collaboration (4) (7). One surprising fact is the degree of standardization reached by all bacteria. Most of them (more than 99%) have one of three basic simple shapes, are about a thousand times smaller than eukaryotic cells and contain about a thousand times less DNA. With few exceptions they are surrounded by a cell-wall whose main rigid component is peptidoglycan for eubacteria, and a more variable but related molecule for archaebacteria. A bacterium contains a minimum number of stable and essential genes, all situated on one relatively large circular DNA molecule: the "chromosome". These genes represent in each bacterium only a minimal fraction of the global bacterial hereditary bioenergetic potential. Far from being a primitive species a type of bacterium is a highly specialized cell, the result of countless trials and reactions to ever changing conditions.
Bacteria and the origin of eukaryotes
Bacteria's associative capacities seem to have favoured, around 1.5 billion years ago, the origin of eukaryotes from the endosymbiosis of three types of bacteria, as proposed in the sequential symbioses theory of the origin of eukaryotes (8). Many of their offspring in the following hundreds of millions of years progressed tremendously by supplementary symbioses with whole bacteria (1) (9) (10). For example, cyanobacteria were added to future algae, lichens and plants which were responsible for the conquest of continents by a new, abundant life, along with nitrogen-fixing bacteria which concentrate nitrogen in the roots of legumes. Rumen bacterial teams help ruminants digest cellulose and many insects and marine animals depend on bacterial symbionts. Several of these associations had crucial impacts on important transitions in evolution. In general, the eukaryotes survived immersed in the middle of the bacterial world and not directly menaced by it. The every day contribution of bacteria to life on Earth is momentous and by ignorance humans may unsettle it with even more catastrophic consequences than resistance to antibiotics.
In conclusion we invite reflection and sollicit comments on the following :
1. Bacterial evolution has been entirely original compared with that of other living beings. It favoured solidarity and interdependence between bacterial cells to the point that they are now operationally (although not structurally) the equivalent of the differentiated cells of an animal or a plant. There is a great genetic variety in bacteria. It is kept in a dynamic state by generalized "horizontal" exchanges added to the "vertical" transfer to siblings. Horizontal exchanges are efficiently done on a temporary basis mostly by self-transmissible plasmids and prophages, the most typically bacterial innovations. Strictly speaking there are no individual bacterial species.
2. Temporary associations of different cells in bacterial teams, and active, generalized exchanges of genes have resulted in a global bacterial communication system which helps bacteria to adapt to changing environmental realities in a computer-like way.
3. Bacteria are the major biological factors in the maintenance of global homeostasis.
4. Bacteria have participated in the origin of eukaryotes and, subsequently, through a number of symbioses have allowed them to realize amazing and momentous evolutionary innovations.
5. Bacteria represent a highly evolved form of life. Taken together they constitute a global superorganism, the most influential biological entity since life exists on our planet. They also were Nature's very first genetic engineers.
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